Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation

Mukhopadhyay, Abhishek; McGuire, Tammy L.; Peng, Chian Yu; Kessler, John A.

doi:10.1242/dev.034439

Cited by 54 publications

(54 citation statements)

References 58 publications

(78 reference statements)

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“…Another gene purported to be highly expressed in the OB, ferritin (Connor et al , 1990) showed little response to CPF, but was induced on exposure to Cu alone, and also by the Cu/CPF mixtures (Figure 4B). The pvalb8 protein is important in maintaining calcium ion balance in neuronal cells (Mukhopadhyay et al , 2009). As observed in figure 5B, expression of the pvalb8 transcript was impacted by CPF, but was much more repressed in the presence of Cu.…”

Section: Resultsmentioning

confidence: 99%

Transcriptional impact of organophosphate and metal mixtures on olfaction: Copper dominates the chlorpyrifos-induced response in adult zebrafish

Tilton

Bammler

et al. 2011

Aquatic Toxicology

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Chemical exposures in fish have been linked to loss of olfaction leading to an inability to detect predators and prey and decreased survival. However, the mechanisms underlying olfactory neurotoxicity are not well characterized, especially in environmental exposures which involve chemical mixtures. We used zebrafish to characterize olfactory transcriptional responses by two model olfactory inhibitors, the pesticide chlorpyrifos (CPF) and mixtures of CPF with the neurotoxic metal copper (Cu). Microarray analysis was performed on RNA from olfactory tissues of zebrafish exposed to CPF alone or to a mixture of CPF and Cu. Gene expression profiles were analyzed using Principal Component Analysis and hierarchical clustering, whereas gene set analysis was used to identify biological themes in the microarray data. Microarray results were confirmed by real-time PCR on genes serving as potential biomarkers of olfactory injury. In addition, we mined our previously published Cu-induced zebrafish olfactory transcriptional response database (Tilton et al., 2008) for the purposes of discriminating pathways of olfaction impacted by either the individual agents or the CPF-Cu mixture transcriptional signatures. CPF exposure altered the expression of gene pathways associated with cellular morphogenesis and odorant binding, but not olfactory signal transduction, a known olfactory pathway for Cu. The mixture profiles shared genes from the Cu and CPF datasets, whereas some genes were altered only by the mixtures. The transcriptional signature of the mixtures was more similar to that in zebrafish exposed to Cu alone then for CPF. In conclusion, exposure to a mixture containing a common environmental metal and pesticide causes a unique transcriptional signature that is heavily influenced by the metal, even when organophosphate predominates. Our findings support using zebrafish microarray analysis to elucidate mechanisms of olfactory loss and to identify the components of mixtures which most strongly contribute to olfactory injury.

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Section: Resultsmentioning

confidence: 99%

Transcriptional impact of organophosphate and metal mixtures on olfaction: Copper dominates the chlorpyrifos-induced response in adult zebrafish

Tilton

Bammler

et al. 2011

Aquatic Toxicology

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“…We found that both types of GABAergic neurons are present at 4M, which indicates that our differentiation protocol generates GABAergic neurons of mixed subtypes. It is possible that an additional step involving the treatment of the differentiating cells with a factor such as BMP4 would lead to a more homogeneous population of GABAergic interneurons expressing PV (Mukhopadhyay et al, 2009). …”

Section: Discussionmentioning

confidence: 99%

All-trans-retinoid acid induces the differentiation of encapsulated mouse embryonic stem cells into GABAergic neurons

Addae

Gernapudi

et al. 2012

Differentiation

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Embryonic stem (ES) cells are pluripotent cells that can differentiate into all three main germ layers: endoderm, mesoderm, and ectoderm. Although a number of methods have been developed to differentiate ES cells into neuronal phenotypes such as sensory and motor neurons, the efficient generation of GABAergic interneurons from ES cells still presents an ongoing challenge. Because the main output of inhibitory GABAergic interneurons is the gamma-aminobutyric-acid (GABA), a neurotransmitter whose controlled homeostasis is required for normal brain function, the efficient generation in culture of functional interneurons may have future implications on the treatment of neurological disorders such as epilepsy, autism, and schizophrenia. The goal of this work was to examine the generation of GABAergic neurons from mouse ES cells by comparing an embryoid body-based methodology versus a hydrogel-based encapsulation protocol that involves the use of all-trans-retinoid acid (RA). We observed that 1) there was a 2-fold increase in neuronal differentiation in encapsulated versus non-encapsulated cells and 2) there was an increase in the specificity for interneuronal differentiation in encapsulated cells, as assessed by mRNA expression and electrophysiology approaches. Furthermore, our results indicate that most of the neurons obtained from encapsulated mouse ES cells are GABA-positive (~87%). Thus, these results suggest that combining encapsulation of ES cells and RA treatment provide a more efficient and scalable differentiation strategy for the generation in culture of functional GABAergic interneurons. This technology may have implications for future cell replacement therapies and the treatment of CNS disorders.

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“…This is evident in the greater number of GABAergic interneurons that are derived from progenitor cells in the dorsolateral versus the dorsomedial wall of the telencephalon, where BMP expression is highest (Furuta et al 1997;Mehler et al 1997;Grove et al 1998). Exogenous Shh expression in the dorsomedial wall enhances the number of GABAergic interneurons (Gulacsi and Lillien 2003), whereas BMP signaling determines the fate of GABAergic interneuron pre-cursors, promoting differentiation of parvalbumin-positive interneurons and blocking differentiation of calbindin-and somatostatinpositive interneurons (Samanta et al 2007;Mukhopadhyay et al 2009). Induction of basal forebrain cholinergic neurons (BFCNs) requires BMP-9 expression (Ló pez-Coviella et al 2000,2005) and, interestingly, human embryonic stem-cell cultures confirm that BMP-9 induces expression of transcription factors that are necessary and sufficient for BFCN induction (Bissonnette et al 2011).…”

Section: Forebrainmentioning

confidence: 99%

TGF-β Family Signaling in Neural and Neuronal Differentiation, Development, and Function

Meyers

Kessler

2017

Cold Spring Harb Perspect Biol

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Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation

Cited by 54 publications

References 58 publications

Transcriptional impact of organophosphate and metal mixtures on olfaction: Copper dominates the chlorpyrifos-induced response in adult zebrafish

Transcriptional impact of organophosphate and metal mixtures on olfaction: Copper dominates the chlorpyrifos-induced response in adult zebrafish

All-trans-retinoid acid induces the differentiation of encapsulated mouse embryonic stem cells into GABAergic neurons

TGF-β Family Signaling in Neural and Neuronal Differentiation, Development, and Function

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